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. 1997 Sep;115(1):273–282. doi: 10.1104/pp.115.1.273

Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism.

D E Godt 1, T Roitsch 1
PMCID: PMC158483  PMID: 9306701

Abstract

The aim of the present study was to gain insight into the contribution of extracellular invertases for sink metabolism in tomato (Lycopersicon esculentum L.). The present study shows that extracellular invertase isoenzymes are encoded by a gene family comprising four members: Lin5, Lin6, Lin7, and Lin8. The regulation of mRNA levels by internal and external signals and the distribution in sink and source tissues has been determined and compared with mRNA levels of the intracellular sucrose (Suc)-cleaving enzymes Suc synthase and vacuolar invertase. The specific regulation of Lin5, Lin6, and Lin7 suggests an important function of apoplastic cleavage of Suc by cell wall-bound invertase in establishing and maintaining sink metabolism. Lin6 is expressed under conditions that require a high carbohydrate supply. The corresponding mRNA shows a sink tissue-specific distribution and the concentration is elevated by stress-related stimuli, by the growth-promoting phytohormone zeatin, and in response to the induction of heterotrophic metabolism. The expression of Lin5 and Lin7 in gynoecia and stamens, respectively, suggests an important function in supplying carbohydrates to these flower organs, whereas the Lin7 mRNA was found to be present exclusively in this specific sink organ.

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Selected References

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  1. Cheng W. H., Taliercio E. W., Chourey P. S. The Miniature1 Seed Locus of Maize Encodes a Cell Wall Invertase Required for Normal Development of Endosperm and Maternal Cells in the Pedicel. Plant Cell. 1996 Jun;8(6):971–983. doi: 10.1105/tpc.8.6.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. DeWald D. B., Sadka A., Mullet J. E. Sucrose Modulation of Soybean Vsp Gene Expression Is Inhibited by Auxin. Plant Physiol. 1994 Feb;104(2):439–444. doi: 10.1104/pp.104.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dorion S., Lalonde S., Saini H. S. Induction of Male Sterility in Wheat by Meiotic-Stage Water Deficit Is Preceded by a Decline in Invertase Activity and Changes in Carbohydrate Metabolism in Anthers. Plant Physiol. 1996 May;111(1):137–145. doi: 10.1104/pp.111.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ehness R., Roitsch T. Co-ordinated induction of mRNAs for extracellular invertase and a glucose transporter in Chenopodium rubrum by cytokinins. Plant J. 1997 Mar;11(3):539–548. doi: 10.1046/j.1365-313x.1997.11030539.x. [DOI] [PubMed] [Google Scholar]
  5. Gruber B., Petchenik L., Williams M., Thomas C., Luken M. G. Malignant vestibular schwannoma. Skull Base Surg. 1994;4(4):227–231. doi: 10.1055/s-2008-1058959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Heim U., Weber H., Bäumlein H., Wobus U. A sucrose-synthase gene of Vicia faba L.: expression pattern in developing seeds in relation to starch synthesis and metabolic regulation. Planta. 1993;191(3):394–401. doi: 10.1007/BF00195698. [DOI] [PubMed] [Google Scholar]
  7. Junghans H., Metzlaff M. A simple and rapid method for the preparation of total plant DNA. Biotechniques. 1990 Feb;8(2):176–176. [PubMed] [Google Scholar]
  8. Klann E. M., Chetelat R. T., Bennett A. B. Expression of Acid Invertase Gene Controls Sugar Composition in Tomato (Lycopersicon) Fruit. Plant Physiol. 1993 Nov;103(3):863–870. doi: 10.1104/pp.103.3.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Klann E., Yelle S., Bennett A. B. Tomato fruit Acid invertase complementary DNA : nucleotide and deduced amino Acid sequences. Plant Physiol. 1992 May;99(1):351–353. doi: 10.1104/pp.99.1.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Leigh R. A., Rees T., Fuller W. A., Banfield J. The location of acid invertase activity and sucrose in the vacuoles of storage roots of beetroot (Beta vulgaris). Biochem J. 1979 Mar 15;178(3):539–547. doi: 10.1042/bj1780539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lingle S. E., Dunlap J. R. Sucrose Metabolism in Netted Muskmelon Fruit during Development. Plant Physiol. 1987 Jun;84(2):386–389. doi: 10.1104/pp.84.2.386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lorenz K., Lienhard S., Sturm A. Structural organization and differential expression of carrot beta-fructofuranosidase genes: identification of a gene coding for a flower bud-specific isozyme. Plant Mol Biol. 1995 Apr;28(1):189–194. doi: 10.1007/BF00042049. [DOI] [PubMed] [Google Scholar]
  13. Martin T., Frommer W. B., Salanoubat M., Willmitzer L. Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolization of sucrose both during phloem loading and in sink organs. Plant J. 1993 Aug;4(2):367–377. doi: 10.1046/j.1365-313x.1993.04020367.x. [DOI] [PubMed] [Google Scholar]
  14. Miller M. E., Chourey P. S. The Maize Invertase-Deficient miniature-1 Seed Mutation Is Associated with Aberrant Pedicel and Endosperm Development. Plant Cell. 1992 Mar;4(3):297–305. doi: 10.1105/tpc.4.3.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Roitsch T., Bittner M., Godt D. E. Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink-source regulation. Plant Physiol. 1995 May;108(1):285–294. doi: 10.1104/pp.108.1.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Salanoubat M., Belliard G. The steady-state level of potato sucrose synthase mRNA is dependent on wounding, anaerobiosis and sucrose concentration. Gene. 1989 Dec 7;84(1):181–185. doi: 10.1016/0378-1119(89)90153-4. [DOI] [PubMed] [Google Scholar]
  17. Sturm A., Chrispeels M. J. cDNA cloning of carrot extracellular beta-fructosidase and its expression in response to wounding and bacterial infection. Plant Cell. 1990 Nov;2(11):1107–1119. doi: 10.1105/tpc.2.11.1107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Sung S. J., Xu D. P., Black C. C. Identification of actively filling sucrose sinks. Plant Physiol. 1989 Apr;89(4):1117–1121. doi: 10.1104/pp.89.4.1117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Truernit E., Schmid J., Epple P., Illig J., Sauer N. The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. Plant Cell. 1996 Dec;8(12):2169–2182. doi: 10.1105/tpc.8.12.2169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Unger C., Hardegger M., Lienhard S., Sturm A. cDNA cloning of carrot (Daucus carota) soluble acid beta-fructofuranosidases and comparison with the cell wall isoenzyme. Plant Physiol. 1994 Apr;104(4):1351–1357. doi: 10.1104/pp.104.4.1351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wang F., Sanz A., Brenner M. L., Smith A. Sucrose Synthase, Starch Accumulation, and Tomato Fruit Sink Strength. Plant Physiol. 1993 Jan;101(1):321–327. doi: 10.1104/pp.101.1.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Weber H., Borisjuk L., Heim U., Buchner P., Wobus U. Seed coat-associated invertases of fava bean control both unloading and storage functions: cloning of cDNAs and cell type-specific expression. Plant Cell. 1995 Nov;7(11):1835–1846. doi: 10.1105/tpc.7.11.1835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Weber H., Buchner P., Borisjuk L., Wobus U. Sucrose metabolism during cotyledon development of Vicia faba L. is controlled by the concerted action of both sucrose-phosphate synthase and sucrose synthase: expression patterns, metabolic regulation and implications for seed development. Plant J. 1996 Jun;9(6):841–850. doi: 10.1046/j.1365-313x.1996.9060841.x. [DOI] [PubMed] [Google Scholar]
  24. Xu J., Avigne W. T., McCarty D. R., Koch K. E. A Similar Dichotomy of Sugar Modulation and Developmental Expression Affects Both Paths of Sucrose Metabolism: Evidence from a Maize Invertase Gene Family. Plant Cell. 1996 Jul;8(7):1209–1220. doi: 10.1105/tpc.8.7.1209. [DOI] [PMC free article] [PubMed] [Google Scholar]

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